Elsevier

Brain and Cognition

Volume 34, Issue 2, July 1997, Pages 218-245
Brain and Cognition

Regular Article
Role of the Striatum, Cerebellum, and Frontal Lobes in the Learning of a Visuomotor Sequence,☆☆,

https://doi.org/10.1006/brcg.1997.0899Get rights and content

Abstract

This study was designed to examine the role of the striatum, cerebellum, and frontal lobes in the implicit learning of a visuomotor sequence. The performance of patients with idiopathic Parkinson's disease (PD), with damage to the cerebellum, or with a circumscribed lesion to the frontal lobes was thus compared to that of separate groups of matched normal control subjects on an adapted version of the Repeated Sequence Test. This paradigm consists of a visual reaction-time task with a fixed embedded sequence of finger movements to be performed based on presentation of visual stimuli. Subjects received four blocks of trials (i.e., 40 presentations of a 10-item sequence) per day over 6 training days. Following the last experimental session, subjects were also given two tests measuring their declarative knowledge of the sequence. Only PD patients with a bilateral striatal-dysfunction or patients with lesions to the cerebellum failed to improve their performance in the last three training sessions, hence suggesting an impairment late in the acquisition process. Further analyses revealed that such impairment was mainly implicit in nature, and that it could not be ascribed to a general decline in cognitive functioning, to mood disturbances, or to the severity of the motor symptoms. By contrast, the level of declarative knowledge of the sequence did not differ between the three clinical groups and their respective groups of normal subjects. These findings suggest that, unlike declarative memory, the incremental acquisition of a new visuomotor skill depends upon the integrity of both the striatum and the cerebellum, but not of the frontal lobes.

References (81)

  • F. Boller et al.

    Visuospatial impairment in Parkinson's disease

    Archives of Neurology

    (1984)
  • M.W. Bondi et al.

    Implicit and explicit memory in Alzheimer's disease and Parkinson's disease

    Journal of Clinical and Experimental Neuropsychology

    (1991)
  • P. Bourque et al.

    Etude psychométrique du questionnaire de dépression de Beck auprès d'un échantillon d'étudiants universitaires francophones

    Revue Canadienne des Sciences du Comportement

    (1982)
  • V.B. Brooks et al.

    Cerebellar control of posture and movement

    Handbook of physiology

    (1981)
  • P. Brotchie et al.

    Motor function of the monkey globus pallidus

    Brain

    (1991)
  • R.G. Brown et al.

    Cognitive functions in Parkinson's disease: From description to theory

    Trends in Neuroscience

    (1990)
  • A.G.M. Canavan et al.

    Conditional associative learning is impaired in cerebellar disease in humans

    Behavioral Neuroscience

    (1994)
  • A. Cohen et al.

    On tasks, knowledge, correlations, and dissociations: Comment on Perruchet and Amorim (1992)

    Journal of Experimental Psychology: Learning, Memory and Cognition

    (1992)
  • A. Cohen et al.

    Attention and structure in sequence learning

    Journal of Experimental Psychology: Learning, Memory and Cognition

    (1990)
  • E. Courchesne

    A neurophysiological view of autism

  • I. Daum et al.

    Declarative and procedural memory in Parkinson's disease

    Movement Disorders

    (1992)
  • I. Divac et al.

    The neostriatum

    (1979)
  • J. Doyon et al.

    Analyse des déficits visuo-spatiaux associés à la maladie de Parkinson

    International Journal of Psychology

    (1996)
  • J. Doyon et al.

    Contribution of the striatum and cerebellum in visuomotor skill learning

    Proceedings of Society for Neuroscience

    (1993)
  • J. Doyon, B. Laforce, D. Gaudreau, M. Castonguay, C. Truchon, G. Bouchard, et al. 1993b, Contribution of the striatum,...
  • J. Doyon et al.

    Functional anatomy of visuomotor skill learning in human subjects using positron emission tomography

    European Journal of Neuroscience

    (1996)
  • B. Dubois et al.

    Cognitive deficits in Parkinson's disease

  • R.F. Ferraro et al.

    Implicit memory and the formation of new associations in nondemented Parkinson's disease individuals and individuals with senile dementia of the Alzheimer type: A serial reaction time (SRT) investigation

    Brain and Cognition

    (1993)
  • J. Fiez et al.

    Impaired non motor learning and error detection associated with cerebellar damage: A single case study

    Brain

    (1992)
  • C. Frith et al.

    Impairment in the learning and performance of a new manual skill in patients with Parkinson's disease

    Journal of Neurology, Neurosurgery, and Neuropsychiatry

    (1986)
  • K.J. Friston et al.

    Motor practice and neurophysiological adaptation in the cerebellum: a positron tomography study

    Proceedings Royal Society London [Biology]

    (1992)
  • G. Goldberg

    Supplementary motor area structure and function: Review and hypotheses

    Behavioral Brain Research

    (1985)
  • A.M. Graybiel et al.

    The basal ganglia and adaptive motor control

    Science

    (1994)
  • D.L. Harrington et al.

    Procedural memory in Parkinson's disease: Impaired motor but not visuoperceptual learning

    Journal of Clinical and Experimental Neuropsychology

    (1990)
  • W.C. Heindel et al.

    Impaired learning of a motor skill in patients with Huntington's disease

    Behavioral Neuroscience

    (1988)
  • W.C. Heindel et al.

    Neuropsychological evidence for multiple implicit memory systems: A comparison of Alzheimer's, Huntington's, and Parkinson's disease patients

    Journal of Neuroscience

    (1989)
  • M.M. Hoehn et al.

    Parkinsonism onset, progression and mortality

    Neurology

    (1967)
  • J.H. Howard et al.

    Serial pattern learning by event observation

    Journal of Experimental Psychology: Learning Memory and Cognition

    (1992)
  • A.W. Inhoff et al.

    The role of cerebellar structures in the execution of serial movements

    Brain

    (1989)
  • M. Ito

    A new physiological concept on cerebellum

    Revue Neurologique

    (1993)
  • Cited by (255)

    View all citing articles on Scopus

    We express our appreciation to the patients and control subjects who participated in the present experiment. Also, we thank Rhonda Amsel for her statistical advice; Dr. Adrian M. Owen, Dr. Viviane Sziklas, Martin Lafleur, and Philip Jackson for their comments on an earlier version of this text; Joanne Roy for her help in many aspects of this research; and Dr. Luc Rousseau and Richard Breton for writing the computer programs. This research was supported in part by grants to Julien Doyon from the Natural Sciences and Engineering Research Council OGPIN 012, and the Fondation de l'Hôpital de l'Enfant-Jésus, Québec city, Canada.

    ☆☆

    Address reprint requests to Julien Doyon, Ph.D., Groupe de Recherche en Réadaptation Physique, Centre Francois-Charon, 525, Boul. Wilfrid-Hamel, Local B-77, Québec, Québec, Canada, G1M 2S8. E-mail: [email protected]. Fax: 418-529-3548.

    J. B. BrookhartV. B. Mountcastle

    View full text